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Natural and chemotherapy-induced clonal evolution of tumors

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Abstract

Evolution and natural selection of tumoral clones in the process of transformation and the following carcinogenesis can be called natural clonal evolution. Its main driving factors are internal: genetic instability initiated by driver mutations and microenvironment, which enables selective pressure while forming the environment for cell transformation and their survival. We present our overview of contemporary research dealing with mechanisms of carcinogenesis in different localizations from precancerous pathologies to metastasis and relapse. It shows that natural clonal evolution establishes intratumoral heterogeneity and enables tumor progression. Tumors of monoclonal origin are of low-level intratumoral heterogeneity in the initial stages, and this increases with the size of the tumor. Tumors of polyclonal origin are of extremely high-level intratumoral heterogeneity in the initial stages and become more homogeneous when larger due to clonal expansion. In cases of chemotherapy-induced clonal evolution of a tumor, chemotherapy becomes the leading factor in treatment. The latest research shows that the impact of chemotherapy can radically increase the speed of clonal evolution and lead to new malignant and resistant clones that cause tumor metastasis. Another option of chemotherapy-induced clonal evolution is formation of a new dominant clone from a clone that was minor in the initial tumor and obtained free space due to elimination of sensitive clones by chemotherapy. As a result, in ~20% of cases, chemotherapy can stimulate metastasis and relapse of tumors due to clonal evolution. The conclusion of the overview formulates approaches to tumor treatment based on clonal evolution: in particular, precision therapy, prediction of metastasis stimulation in patients treated with chemotherapy, methods of genetic evaluation of chemotherapy efficiency and clonal-oriented treatment, and approaches to manipulating the clonal evolution of tumors are presented.

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References

  1. Nowell, P. C. (1976) The clonal evolution of tumor cell populations, Science, 194, 23–28.

    Article  CAS  PubMed  Google Scholar 

  2. Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., Martinez, P., Matthews, N., Stewart, A., Tarpey, P., Varela, I., Phillimore, B., Begum, S., McDonald, N. Q., Butler, A., Jones, D., Raine, K., Latimer, C., Santos, C. R., Nohadani, M., Eklund, A. C., Spencer-Dene, B., Clark, G., Pickering, L., Stamp, G., Gore, M., Szallasi, Z., Downward, J., Futreal, P. A., and Swanton, C. (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing, New Eng. J. Med., 366, 883–892.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Krakhmal, N. V., Zavyalova, M. V., Denisov, E. V., Vtorushin, S. V., and Perelmuter, V. M. (2015) Cancer invasion: patterns and mechanisms, Acta Naturae, 72, 17–28.

    Google Scholar 

  4. Gerashchenko, T. S., Denisov, E. V., Litviakov, N. V., Zavyalova, M. V., Vtorushin, S. V., Tsyganov, M. M., Perelmuter, V. M., and Cherdyntseva, N. V. (2013) Intratumor heterogeneity: nature and biological significance, Biochemistry (Moscow), 78, 1201–1215.

    Article  CAS  Google Scholar 

  5. Bhatia, S., Frangioni, J. V., Hoffman, R. M., Iafrate, A. J., and Polyak, K. (2012) The challenges posed by cancer heterogeneity, Nat. Biotechnol., 30, 604–610.

    Article  CAS  PubMed  Google Scholar 

  6. Visvader, J. E. (2011) Cells of origin in cancer, Nature, 469, 314–322.

    Article  CAS  PubMed  Google Scholar 

  7. Marusyk, A., and Polyak, K. (2010) Tumor heterogeneity: causes and consequences, Biochim. Biophys. Acta, 1805, 105–117.

    CAS  PubMed  Google Scholar 

  8. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation, Cell, 144, 646–674.

    Article  CAS  PubMed  Google Scholar 

  9. Zavyalova, M. V., Perelmuter, V. M., Vtorushin, S. V., Denisov, E. V., Litvyakov, N. V., Slonimskaya, E. M., and Cherdyntseva, N. V. (2013) The presence of alveolar structures in invasive ductal NOS breast carcinoma is associated with lymph node metastasis, Diagn. Cytopathol., 41, 279282.

    Article  Google Scholar 

  10. Van Niekerk, G., Davids, L. M., Hattingh, S. M., and Engelbrecht, A. M. (2016) Cancer stem cells: a product of clonal evolution? Int. J. Cancer, 140, 993–999.

    Article  PubMed  Google Scholar 

  11. Devarakonda, S., and Govindan, R. (2015) Clonal evolution: multiregion sequencing of esophageal adenocarcinoma before and after chemotherapy, Cancer Discov., 5, 796798.

    Article  Google Scholar 

  12. Fisher, R., Pusztai, L., and Swanton, C. (2013) Cancer heterogeneity: implications for targeted therapeutics, Br. J. Cancer, 108, 479–485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Cross, W., Graham, T. A., and Wright, N. A. (2016) New paradigms in clonal evolution: punctuated equilibrium in cancer, J. Pathol., 240, 126–136.

    Article  PubMed  Google Scholar 

  14. Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., Ramakrishna, M., Shlien, A., Cooke, S. L., Hinton, J., Menzies, A., Stebbings, L. A., Leroy, C., Jia, M., Rance, R., Mudie, L. J., Gamble, S. J., Stephens, P. J., McLaren, S., Tarpey, P. S., Papaemmanuil, E., Davies, H. R., Varela, I., McBride, D. J., Bignell, G. R., Leung, K., Butler, A. P., Teague, J. W., Martin, S., Jonsson, G., Mariani, O., Boyault, S., Miron, P., Fatima, A., Langerod, A., Aparicio, S. A., Tutt, A., Sieuwerts, A. M., Borg, A., Thomas, G., Salomon, A. V., Richardson, A. L., BorresenDale, A. L., Futreal, P. A., Stratton, M. R., and Campbell, P. J.; Breast Cancer Working Group of the International Cancer Genome Consortium (2012) The life history of 21 breast cancers, Cell, 149, 994–1007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Navin, N., Krasnitz, A., Rodgers, L., Cook, K., Meth, J., Kendall, J., Riggs, M., Eberling, Y., Troge, J., Grubor, V., Levy, D., Lundin, P., Maner, S., Zetterberg, A., Hicks, J., and Wigler, M. (2010) Inferring tumor progression from genomic heterogeneity, Genome Res., 20, 68–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ng, C. K., Pemberton, H. N., and Reis-Filho, J. S. (2014) Breast cancer intratumor genetic heterogeneity: causes and implications, Exp. Rev. Anticancer Ther., 12, 1021–1032.

    Article  Google Scholar 

  17. Stephens, P. J., Tarpey, P. S., Davies, H., Van, Loo P., Greenman, C., Wedge, D. C., Nik-Zainal, S., Martin, S., Varela, I., Bignell, G. R., Yates, L. R., Papaemmanuil, E., Beare, D., Butler, A., Cheverton, A., Gamble, J., Hinton, J., Jia, M., Jayakumar, A., Jones, D., Latimer, C., Lau, K. W., McLaren, S., McBride, D. J., Menzies, A., Mudie, L., Raine, K., Rad, R., Chapman, M. S., Teague, J., Easton, D., Langerod, A., Lee, M. T., Shen, C. Y., Tee, B. T., Huimin, B. W., Broeks, A., Vargas, A. C., Turashvili, G., Martens, J., Fatima, A., Miron, P., Chin, S. F., Thomas, G., Boyault, S., Mariani, O., Lakhani, S. R., Van de Vijver, M., Van’t Veer, L., Foekens, J., Desmedt, C., Sotiriou, C., Tutt, A., Caldas, C., Reis-Filho, J. S., Aparicio, S. A., Salomon, A. V., Borresen-Dale, A. L., Richardson, A. L., Campbell, P. J., Futreal, P. A., Stratton, M. R., and Oslo Breast Cancer Consortium (OSBREAC) (2012) The landscape of cancer genes and mutational processes in breast cancer, Nature, 486, 400–404.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Alexandrov, L. B., Nik-Zainal, S., Wedge, D. C., Aparicio, S. A. J. R., Behjati, S., Biankin, A. V., Bignell, G. R., Bolli, N., Borg, A., Borresen-Dale, A.-L., Boyault, S., Burkhardt, B., Butler, A. P., Caldas, C., Davies, H. R., Desmedt, C., Eils, R., Eyfjord, J. E., Foekens, J. A., Greaves, M., Hosoda, F., Hutter, B., Ilicic, T., Imbeaud, S., Imielinsk, M., Jager, N., Jones, D. T. W., Jones, D., Knappskog, S., Kool, M., Lakhani, S. R., Lopez-Otin, C., Martin, S., Munshi, N. C., Nakamura, H., Northcott, P. A., Pajic, M., Papaemmanuil, E., Paradiso, A., Pearson, J. V., Puente, X. S., Raine, K., Ramakrishna, M., Richardson, A. L., Richter, J., Rosenstiel, P., Schlesner, M., Schumacher, T. N., Span, P. N., Teague, J. W., Totoki, Y., Tutt, A. N. J., Valdes-Mas, R., van Buuren, M. M., Van’t Veer, L., Vincent-Salomon, A., Waddell, N., Yates, L. R., Australian Pancreatic Cancer Genome Initiative, ICGC Breast Cancer Consortium, ICGC MMML-Seq Consortium, ICGC PedBrain, Zucman-Rossi, J., Futreal, P. A., McDermott, U., Lichter, P., Meyerson, M., Grimmond, S. M., Siebert, R., Campo, E., Shibata, T., Pfister, S. M., Campbell, P. J., and Stratton, M. R. (2013) Signatures of mutational processes in human cancer, Nature, 500, 415–421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bhatia, S., Frangioni, J. V., Hoffman, R. M., Iafrate, A. J., and Polyak, K. (2012) The challenges posed by cancer heterogeneity, Nat. Biotechnol., 30, 604–610.

    Article  CAS  PubMed  Google Scholar 

  20. Greaves, M., and Maley, C. C. (2012) Clonal evolution in cancer, Nature, 481, 306–313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. McGranahan, N., and Swanton, C. (2015) Biological and therapeutic impact of intratumor heterogeneity in cancer evolution, Cancer Cell, 27, 15–26.

    Article  CAS  PubMed  Google Scholar 

  22. Michor, F., and Polyak, K. (2010) The origins and implications of intratumor heterogeneity, Cancer Prevent. Res., 3, 1361–1364.

    Article  Google Scholar 

  23. Greaves, M., and Ford, A. M. (2015) Chromosome translocations, cancer initiation and clonal evolution, in Chromosomal Translocations and Genome Rearrangements in Cancer (Rowley, J. D., Le Beau, M. M., and Rabbitts, T. H., eds.), Springer, pp. 53–72.

    Chapter  Google Scholar 

  24. Giancotti, F. G. (2013) Mechanisms governing metastatic dormancy and reactivation, Cell, 155, 750–764.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Apostoli, A. J., and Ailles, L. (2016) Clonal evolution and tumor-initiating cells: new dimensions in cancer patient treatment, Crit. Rev. Clin. Lab. Sci., 53, 40–51.

    Article  CAS  PubMed  Google Scholar 

  26. Almendro, V., Marusyk, A., and Polyak, K. (2013) Cellular heterogeneity and molecular evolution in cancer, Annu. Rev. Pathol. Mech. Dis., 8, 277–302.

    Article  CAS  Google Scholar 

  27. Almendro, V., Kim, H. J., Cheng, Y.-K., Gonen, M., Itzkovitz, S., Argani, P., Van Oudenaarden, A., Sukumar, S., Michor, F., and Polyak, K. (2014) Genetic and phenotypic diversity in breast tumor metastases, Cancer Res., 74, 1338–1348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Polyak, K. (2014) Tumor heterogeneity confounds and illuminates: a case for Darwinian tumor evolution, Nat. Med., 20, 344–346.

    Article  CAS  PubMed  Google Scholar 

  29. Cho, S. Y., Xu, M., Roboz, J., Lu, M., Mascarenhas, J., and Hoffman, R. (2010) The effect of CXCL12 processing on CD34+ cell migration in myeloproliferative neoplasms, Cancer Res., 70, 3402–3410.

    Article  CAS  PubMed  Google Scholar 

  30. Verstovsek, S., Kantarjian, H., Mesa, R. A., Pardanani, A. D., Cortes-Franco, J., Thomas, D. A., Estrov, Z., Fridman, J. S., Bradley, E. C., Erickson-Viitanen, S., Vaddi, K., Levy, R., and Tefferi, A. (2010) Safety and efficacy of INCB018424, a JAK1 and JAK2 inhibitor, in myelofibrosis, New Eng. J. Med., 363, 1117–1127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Tefferi, A., Thiele, J., Vannucchi, A., and Barbui, T. (2014) An overview on CALR and CSF3R mutations and a proposal for revision of WHO diagnostic criteria for myeloproliferative neoplasms, Leukemia, 28, 1407–1413.

    Article  CAS  PubMed  Google Scholar 

  32. Tefferi, A., Vaidya, R., Caramazza, D., Finke, C., Lasho, T., and Pardanani, A. (2011) Circulating interleukin (IL)-8, IL-2R, IL-12, and IL-15 levels are independently prognostic in primary myelofibrosis: a comprehensive cytokine profiling study, J. Clin. Oncol., 29, 1356–1363.

    Article  CAS  PubMed  Google Scholar 

  33. Thomas, L. K., Bermejo, J. L., Vinokurova, S., Jensen, K., Bierkens, M., Steenbergen, R., Bergmann, M., von Knebel Doeberitz, M., and Reuschenbach, M. (2014) Chromosomal gains and losses in human papillomavirusassociated neoplasia of the lower genital tract–a systematic review and meta-analysis, Eur. J. Cancer, 50, 85–98.

    Article  CAS  PubMed  Google Scholar 

  34. Luhn, P., Houldsworth, J., Cahill, L., Schiffman, M., Castle, P. E., Zuna, R. E., Dunn, S. T., Gold, M. A., Walker, J., and Wentzensen, N. (2013) Chromosomal gains measured in cytology samples from women with abnormal cervical cancer screening results, Gynecol. Oncol., 130, 595600.

    Article  Google Scholar 

  35. Murphy, B. J., Dorudi, S., and Bustin, S. A. (2007) Molecular staging of colorectal cancer: new paradigm or waste of time? Exp. Opin. Med. Diagn., 1, 31–45.

    Article  CAS  Google Scholar 

  36. Sowalsky, A. G., Ye, H., Bubley, G. J., and Balk, S. P. (2013) Clonal progression of prostate cancers from Gleason grade 3 to grade 4, Cancer Res., 73, 1050–1055.

    Article  CAS  PubMed  Google Scholar 

  37. Campbell, P. J., Yachida, S., Mudie, L. J., Stephens, P. J., Pleasance, E. D., Stebbings, L. A., Morsberger, L. A., Latimer, C., McLaren, S., and Lin, M.-L. (2010) The patterns and dynamics of genomic instability in metastatic pancreatic cancer, Nature, 467, 1109–1113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Makohon-Moore, A. P., Zhang, M., Reiter, J. G., Bozic, I., Wong, F., Jiao, Y., Chatterjee, K., Nowak, M., Papadopoulos, N., and Vogelstein, B. (2015) Clonal evolution defines the natural history of metastatic pancreatic cancer, Cancer Res., 75, 4137–4137.

    Article  Google Scholar 

  39. Li, X., Galipeau, P. C., Paulson, T. G., Sanchez, C. A., Arnaudo, J., Liu, K., Sather, C. L., Kostadinov, R. L., Odze, R. D., and Kuhner, M. K. (2014) Temporal and spatial evolution of somatic chromosomal alterations: a casecohort study of Barrett’s esophagus, Cancer Prevent. Res., 7, 114–127.

    Article  Google Scholar 

  40. Aparicio, S., and Caldas, C. (2013) The implications of clonal genome evolution for cancer medicine, New Eng. J. Med., 368, 842–851.

    Article  CAS  PubMed  Google Scholar 

  41. Shah, S. P., Roth, A., Goya, R., Oloumi, A., Ha, G., Zhao, Y., Turashvili, G., Ding, J., Tse, K., and Haffari, G. (2012) The clonal and mutational evolution spectrum of primary triple-negative breast cancers, Nature, 486, 395–399.

    CAS  PubMed  Google Scholar 

  42. Wang, Y., Waters, J., Leung, M. L., Unruh, A., Roh, W., Shi, X., Chen, K., Scheet, P., Vattathil, S., and Liang, H. (2014) Clonal evolution in breast cancer revealed by single nucleus genome sequencing, Nature, 512, 155–160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zavyalova, M. V., Denisov, E. V., Tashireva, L. A., Gerashchenko, T. S., Litviakov, N. V., Skryabin, N. A., Vtorushin, S. V., Telegina, N. S., Slonimskaya, E. M., and Cherdyntseva, N. V. (2013) Phenotypic drift as a cause for intratumoral morphological heterogeneity of invasive ductal breast carcinoma not otherwise specified, Bio Res. Open Access, 2, 148–154.

    Article  Google Scholar 

  44. Denisov, E. V., Litviakov, N. V., Zavyalova, M. V., Perelmuter, V. M., Vtorushin, S. V., Tsyganov, M. M., Gerashchenko, T. S., Garbukov, E. Y., Slonimskaya, E. M., and Cherdyntseva, N. V. (2014) Intratumoral morphological heterogeneity of breast cancer: neoadjuvant chemotherapy efficiency and multidrug resistance gene expression, Sci. Rep., 4, 1–7.

    Article  Google Scholar 

  45. Eirew, P., Steif, A., Khattra, J., Ha, G., Yap, D., Farahani, H., Gelmon, K., Chia, S., Mar, C., and Wan, A. (2015) Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution, Nature, 518, 422426.

    Google Scholar 

  46. Janiszewska, M., and Polyak, K. (2015) Clonal evolution in cancer: a tale of twisted twines, Cell Stem Cell, 16, 11–12.

    Article  CAS  PubMed  Google Scholar 

  47. Marusyk, A., Almendro, V., and Polyak, K. (2012) Intratumour heterogeneity: a looking glass for cancer? Nat. Rev. Cancer, 12, 323–334.

    Article  CAS  PubMed  Google Scholar 

  48. Nik-Zainal, S., Van Loo, P., Wedge, D. C., Alexandrov, L. B., Greenman, C. D., Lau, K. W., Raine, K., Jones, D., Marshall, J., and Ramakrishna, M. (2012) The life history of 21 breast cancers, Cell, 149, 994–1007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Kreso, A., and Dick, J. E. (2014) Evolution of the cancer stem cell model, Cell Stem Cell, 14, 275–291.

    Article  CAS  PubMed  Google Scholar 

  50. Ding, L., Ley, T. J., Larson, D. E., Miller, C. A., Koboldt, D. C., Welch, J. S., Ritchey, J. K., Young, M. A., Lamprecht, T., and McLellan, M. D. (2012) Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing, Nature, 481, 506–510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Keats, J. J., Chesi, M., Egan, J. B., Garbitt, V. M., Palmer, S. E., Braggio, E., Van Wier, S., Blackburn, P. R., Baker, A. S., and Dispenzieri, A. (2012) Clonal competition with alternating dominance in multiple myeloma, Blood, 120, 1067–1076.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Jiang, Y., Redmond, D., Nie, K., Eng, K. W., Clozel, T., Martin, P., Tan, L. H., Melnick, A. M., Tam, W., and Elemento, O. (2014) Deep sequencing reveals clonal evolution patterns and mutation events associated with relapse in B-cell lymphomas, Gen. Biol., 15, 412–420.

    Article  Google Scholar 

  53. Oshima, K., Khiabanian, H., Da Silva-Almeida, A. C., Tzoneva, G., Abate, F., Ambesi-Impiombato, A., SanchezMartin, M., Carpenter, Z., Penson, A., and Perez-Garcia, A. (2016) Mutational landscape, clonal evolution patterns, and role of RAS mutations in relapsed acute lymphoblastic leukemia, PNAS, 201608420.

    Google Scholar 

  54. Malcikova, J., Stano-Kozubik, K., Tichy, B., Kantorova, B., Pavlova, S., Tom, N., Radova, L., Smardova, J., Pardy, F., and Doubek, M. (2015) Detailed analysis of therapydriven clonal evolution of TP53 mutations in chronic lymphocytic leukemia, Leukemia, 29, 877–885.

    Article  CAS  PubMed  Google Scholar 

  55. Johnson, B. E., Mazor, T., Hong, C., Barnes, M., Aihara, K., McLean, C. Y., Fouse, S. D., Yamamoto, S., and Ueda, H. (2014) Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma, Science, 343, 189193.

    Google Scholar 

  56. Wu, X., Northcott, P. A., Dubuc, A., Dupuy, A. J., Shih, D. J. H., Witt, H., Croul, S., Bouffet, E., Fults, D. W., and Eberhart, C. G. (2012) Clonal selection drives genetic divergence of metastatic medulloblastoma, Nature, 482, 529–533.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Gonzalez, D., Martinez, P., Wade, R., Hockley, S., Oscier, D., Matutes, E., Dearden, C. E., Richards, S. M., Catovsky, D., and Morgan, G. J. (2011) Mutational status of the TP53 gene as a predictor of response and survival in patients with chronic lymphocytic leukemia: results from the LRF CLL4 trial, J. Clin. Oncol., 29, 2223–2229.

    Article  PubMed  Google Scholar 

  58. Landau, D. A., Tausch, E., Bttcher, S., Stewart, C., Bozic, I., Leischner, I., Rosebrock, D., Taylor-Weiner, A., Mertens, D., and Sougnez, C. (2015) Quantitative clonal dynamics define mechanisms of CLL evolution in response to combination chemotherapy, Blood, 126, 362–362.

    Google Scholar 

  59. Wang, J., Cazzato, E., Ladewig, E., Frattini, V., Rosenbloom, D. I., Zairis, S., Abate, F., Liu, Z., Elliott, O., and Shin, Y.-J. (2016) Clonal evolution of glioblastoma under therapy, Nat. Genet., 48, 768–796.

    Article  CAS  PubMed  Google Scholar 

  60. Chen, Z.-Y., Zhong, W.-Z., Zhang, X.-C., Su, J., Yang, X.N., Chen, Z.-H., Yang, J.-J., Zhou, Q., Yan, H.-H., and An, S.-J. (2012) EGFR mutation heterogeneity and the mixed response to EGFR tyrosine kinase inhibitors of lung adenocarcinomas, Oncologist, 17, 978–985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Cheng, X., and Chen, H. (2014) Tumor heterogeneity and resistance to EGFR-targeted therapy in advanced nonsmall cell lung cancer: challenges and perspectives, Onco Targets Ther., 7, 1689–1704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Murugaesu, N., Wilson, G. A., Birkbak, N. J., Watkins, T. B., McGranahan, N., Kumar, S., Abbassi-Ghadi, N., Salm, M., Mitter, R., and Horswell, S. (2015) Tracking the genomic evolution of esophageal adenocarcinoma through neoadjuvant chemotherapy, Cancer Discov., 8, 821–831.

    Article  Google Scholar 

  63. Findlay, J. M., Castro-Giner, F., Makino, S., Rayner, E., Kartsonaki, C., Cross, W., Kovac, M., Ulahannan, D., Palles, C., and Gillies, R. S. (2016) Differential clonal evolution in oesophageal cancers in response to neo-adjuvant chemotherapy, Nat. Commun., 7, 1–13.

    Article  Google Scholar 

  64. Kreso, A., O’brien, C. A., van Galen, P., Gan, O. I., Notta, F., Brown, A. M., Ng, K., Ma, J., Wienholds, E., and Dunant, C. (2013) Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer, Science, 339, 543–548.

    Article  CAS  PubMed  Google Scholar 

  65. Diaz, L. A., Jr., Williams, R. T., Wu, J., Kinde, I., Hecht, J. R., Berlin, J., Allen, B., Bozic, I., Reiter, J. G., and Nowak, M. A. (2012) The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers, Nature, 486, 537–540.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Misale, S., Yaeger, R., Hobor, S., Scala, E., Janakiraman, M., Liska, D., Valtorta, E., Schiavo, R., Buscarino, M., and Siravegna, G. (2012) Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer, Nature, 486, 532–536.

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Prandi, D., Baca, S. C., Romanel, A., Barbieri, C. E., Mosquera, J.-M., Fontugne, J., Beltran, H., Sboner, A., Garraway, L. A., Rubin, M. A., and Demichelis, F. (2014) Unraveling the clonal hierarchy of somatic genomic aberrations, Gen. Biol., 15, 439–450.

    Article  Google Scholar 

  68. Litviakov, N., Cherdyntseva, N., Ibragimova, M., Tsyganov, M., Kazantseva, P., Kzhyshkowska, J., and Slonimskaya, E. (2015) 299P: The clonal evolution of a breast tumor during neoadjuvant chemotherapy and metastasis, Ann. Oncol., 27, Suppl. 6, vi94.

    Google Scholar 

  69. Jiang, Y.-Z., Yu, K.-D., Bao, J., Peng, W.-T., and Shao, Z.M. (2014) Favorable prognostic impact in loss of TP53 and PIK3CA mutations after neoadjuvant chemotherapy in breast cancer, Cancer Res., 74, 3399–3407.

    Article  CAS  PubMed  Google Scholar 

  70. Hughes, A. E., Magrini, V., Demeter, R., Miller, C. A., Fulton, R., Fulton, L. L., Eades, W. C., Elliott, K., Heath, S., Westervelt, P., Ding, L., Conrad, D. F., White, B. S., Shao, J., Link, D. C., DiPersio, J. F., Mardis, E. R., Wilson, R. K., Ley, T. J., Walter, M. J., and Graubert, T. A. (2014) Clonal architecture of secondary acute myeloid leukemia defined by single-cell sequencing, PLoS Genet., 10, e1004462.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Gundem, G., Van Loo, P., Kremeyer, B., Alexandrov, L. B., Tubio, J. M., Papaemmanuil, E., Brewer, D. S., Kallio, H. M., Hognas, G., Annala, M., Kivinummi, K., Goody, V., Latimer, C., O’ Meara, S., Dawson, K. J., Isaacs, W., Emmert-Buck, M. R., Nykter, M., Foster, C., Kote-Jarai, Z., Easton, D., Whitaker, H. C., Neal, D. E., Cooper, C. S., Eeles, R. A., Visakorpi, T., Campbell, P. J., McDermott, U., Wedge, D. C., Bova, G. S., and ICGC Prostate UK Group (2015) The evolutionary history of lethal metastatic prostate cancer, Nature, 520, 353–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Naxerova, K., and Jain, R. K. (2015) Using tumour phylogenetics to identify the roots of metastasis in humans, Nat. Rev. Clin. Oncol., 12, 258–272.

    Article  CAS  PubMed  Google Scholar 

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  1. Cancer Research Institute, Tomsk National Research Medical Center of the Russian Academy of Sciences, 634050, Tomsk, Russia

    M. K. Ibragimova, M. M. Tsyganov & N. V. Litviakov

  2. National Research Tomsk State University, 634050, Tomsk, Russia

    M. K. Ibragimova, M. M. Tsyganov & N. V. Litviakov

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  1. M. K. Ibragimova
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  2. M. M. Tsyganov
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  3. N. V. Litviakov
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Correspondence to N. V. Litviakov.

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Original Russian Text © M. K. Ibragimova, M. M. Tsyganov, N. V. Litviakov, 2017, published in Biokhimiya, 2017, Vol. 82, No. 4, pp. 572-586.

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Ibragimova, M.K., Tsyganov, M.M. & Litviakov, N.V. Natural and chemotherapy-induced clonal evolution of tumors. Biochemistry Moscow 82, 413–425 (2017). https://doi.org/10.1134/S0006297917040022

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  • DOI: https://doi.org/10.1134/S0006297917040022

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